Variability in magnesium content in Arctic echinoderm skeletons

Marine Environmental Research xxx (2017) 1e12

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Variability in magnesium content in Arctic echinoderm skeletons
ski a A. Iglikowska a, *, J. Najorka b, A. Voronkov c, M. Chełchowski a, P. Kuklin
co
w Warszawy 55, 81-712, Sopot, Poland Marine Ecology Department, Institute of Oceanology Polish Academy of Sciences, Powstan Core Research Laboratories, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK c Institute of Marine Research, N-9294, Tromsø, Norway a

b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 March 2017 Received in revised form 2 June 2017 Accepted 3 June 2017 Available online xxx

In this study, 235 measurements of magnesium concentration in echinoderm's skeletons were compiled, including 30 species and 216 specimens collected from northern and western Barents Sea. We aimed to reveal the scale of Mg variation in the skeletons of Arctic echinoderms. Furthermore, we attempted to examine whether the Mg concentration in echinoderm skeletons is determined primarily by biological factors or is a passive result of environmental influences. We found that the Mg concentration in echinoderm skeletons was characteristic for particular echinoderm classes or was even species-specific. The highest Mg contents were observed in asteroids, followed by ophiuroids, crinoids, and holothuroids, with the lowest values in echinoids. These results strongly imply that biological factors play an important role in controlling the incorporation of Mg into the skeletons of the studied individuals. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Arctic calcifiers Mg-calcite Skeletal magnesium Ocean acidification Asteroidea Ophiuroidea Echinoidea Holothuroidea Crinoidea Barents sea

1. Introduction Echinoderms are numerous and widely distributed benthic organisms that are important components of marine ecosystems. In the Arctic seas, Echinodermata are often dominant invertebrates, having a large contribution to the remineralisation and redistribution of organic carbon (Renaud et al., 2007; Blicher and Sejr, 2011; Jørgensen et al., 2015). Moreover, they are involved in global cycles of other major (e.g. sulphur, phosphorus, calcium) and minor (e.g. magnesium, strontium, iron) elements. The endoskeleton of most echinoderms consists of a fenestrate lattice of calcium carbonate, called stereom, which is interpenetrated with organic mesodermal tissue (Towe, 1967). The echinoderm biomineralisation strategy is the initial formation of amorphous calcium carbonate (ACC) precursors, that subsequently transform into crystalline phases. The final mineral phase of the skeleton is made

* Corresponding author. E-mail addresses: [email protected] (A. Iglikowska), [email protected] (J. Najorka), [email protected] (A. Voronkov), [email protected]
ski). (M. Chełchowski), [email protected] (P. Kuklin

of magnesium-rich calcite and ~0.1 wt% (percentage by weight) of occluded organic molecules (e.g. Weiner, 1985; Dubois and Chen, 1989). This organic material plays a crucial role in transient stabilization of ACC (e.g. Politi et al., 2004), controlling crystal growth (Berman et al., 1988; Ameye et al., 2001) and modulation of magnesium content (e.g. Hermans et al., 2011). In aquatic environments, magnesium (Mg) is a common additive in biogenic carbonate minerals. Among echinoderms, the amount of Mg in skeletons can vary, and calcitic skeletons are subdivided into low-Mg calcite (0e5 mol% MgCO3), intermediate-Mg calcite (5e8 mol%) and high-Mg calcite (>8 mol%) (Morrison and Brand, 1986). High-Mg calcite, with magnesium concentrations higher than 10 mol%, is known to be a thermodynamically unstable polymorph under ambient conditions (Raz et al., 2000). Synthetic high-Mg calcite can be precipitated only under high temperature and high pressure (Long et al., 2014), although marine invertebrates are often able to produce this unstable phase of calcium carbonate under conditions of modern seawater. Magnesium is incorporated into carbonate minerals by direct substitution for calcium in the CaCO3 crystal structure (Morrison and Brand, 1986). For echinoderms, the potential sources of

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magnesium are food (Asnaghi et al., 2014) and ambient seawater. Nakano et al. (1963) and Lewis et al. (1990) showed with radioactive calcium that, in echinoderm skeletal calcite, calcium is derived from seawater, and magnesium has likely the same origin. The Mg/Ca ratio of modern seawater is z 5.2 (Stanley and Hardie, 1998) therefore, the inorganic precipitation of high-Mg calcite should be favoured (Mackenzie et al., 1983). However, aragonite precipitation occurs more readily since Mg ions inhibit calcite precipitation (Morse, 1983: “Mg poisoning effect”). Crystallisation of high-Mg calcite is therefore only possible in the presence of organic additives, such as citric and malic acids, which are known to enhance the secretion of (magnesian) calcite in magnesium-rich calcifying fluid. The addition of Mg to the medium where crystallisation occurs provides new morphological possibilities, although the role of Mg ions in determining the morphology of calcite crystals is less clear (Meldrum and Hyde, 2001). Pure calcite is extremely brittle as a single crystal (Long et al., 2014). The precipitation of high-Mg calcite, which is a composite of inorganic ions and biomolecules in invertebrate skeletons, greatly enhances the mechanical properties of calcium carbonates. The hardness, stiffness and elastic modulus are demonstrated to be higher for Mg-bearing calcite than for pure synthetic calcite (Ma et al., 2008). Even relatively low concentrations of Mg (z1 mol%) in calcite play a significant role in hardening crystalline calcium carbonate (Kunitake et al., 2012). Additionally, the enhanced mechanical properties of high-Mg calcite are strongly linked to such structural features as the presence of macromolecules, occlusion of Mg ions and crystal orientation (Long et al., 2014). In the calcitic skeletons of echinoderms, magnesium is the most abundant minor element and may vary from 3.0 to 43.5 mol % MgCO3 (Schroeder et al., 1969). The variation in Mg concentration may occur on different levels, such as the variation among particular ossicles within a single specimen or differences among species or higher taxonomic levels. Most marine invertebrates can exert biological control on the magnesium uptake into hard skeletal parts, and this process can lead to enrichment or depletion of the element in skeletal carbonate (Morrison and Brand, 1986). Echinodermata demonstrate strong physiological control on skeletal Mg content (e.g. Chave, 1954; Weber and Raup, 1966; Weber, 1969, 1973; Ebert, 2007), although several studies report that the skeletal Mg/Ca ratio may be shaped, to some extent, by the water temperature (e.g. Clarke and Wheeler, 1917; Chave, 1954; Weber, 1969; Hermans et al., 2010), salinity (e.g. Pilkey and Hower, 1960; Borremans et al., 2009) and the Mg/Ca ratio of ambient seawater (e.g. Dickson, 2002, 2004; Ries, 2004; Hasiuk and Lohmann, 2010). Thus, the final chemical composition of the skeleton is a result of biological control, organism-environment interactions and physiochemical properties of the surrounding seawater. The knowledge of the factors controlling Mg incorporation into biogenic minerals is widely used to infer the mineral growth conditions and thus has important applications in palaeoecological and geochemical studies. Species bearing magnesium-rich skeletons are on the list of the most vulnerable to the effects of climate change and ocean acidification because higher magnesium levels in calcite are strongly correlated to higher solubility under modern seawater conditions. The calcitic skeletons of echinoderms are sometimes well preserved in fossil records; therefore, the Mg content in fossil echinoderms can be used as a proxy for ancient seawater Mg concentrations or temperatures (Dickson, 2002, 2004; Ries, 2004).

Recently, the Arctic Ocean ecosystem has been changing rapidly as a result of climate warming, increased emissions of atmospheric CO2 and anthropogenic activities. The reduction in sea ice coverage causes a substantial increase in CO2 air-sea flux and light availability, thus making the growing season longer and more intense. In addition, the increased Arctic river input and coastal erosion (e.g. Peterson et al., 2002; Mars and Houseknecht, 2007) contribute to an increased nutrient supply, influencing €m primary productivity, particularly in the shelf area (Jutterstro and Anderson, 2010). In the Arctic, the bottom salinity and water temperatures seem to be relatively stable, although changes in primary productivity may significantly change the seawater CO2 concentration and carbonate saturation state, which can potentially affect skeletal precipitation in Arctic calcifiers. Arctic, cold-water and less calcium carbonate-saturated seawater conditions are generally more unfavourable for calcifying organisms, especially for those producing high-Mg calcite, and progressing ocean acidification makes the process of calcification more difficult (e.g. Andersson et al., 2008). Although the Arctic Ocean is changing on an unprecedented scale, our understanding of the effects of these changes on the living part of this unique system is far from satisfactory. To date, there have been only a few studies dealing with biomineralisation problems in the Arctic, which are based on the larger database (e.g. Andersson et al., 2008; Lebrato et al., 2013; Iglikowska et al., 2017). Arctic ecosystem changes are progressing quickly; therefore, there is an urgent need to expand and complete our knowledge regarding the precipitation and properties of calcified skeletons in Arctic invertebrates. The objective of this paper is to reveal the scale of Mg variation in the calcitic skeletons of Arctic echinoderms. In addition to building comprehensive knowledge about Mg concentrations within these skeletons, we test whether the levels of Mg in the skeletons of particular species are species or group specific. The investigated species were often from the same location and were under the influence of the same environmental conditions. We assume that species having different Mg concentrations and therefore having species-specific Mg content in the skeleton would indicate the biological control of Mg incorporation. Based on samples collected across a large spatial scale, where stations differed in environmental conditions, we also test whether the concentrations of Mg in the skeleton of particular species are related to environmental variables (e.g. depth). In this case, we assumed that skeletal Mg concentrations following the same pattern as environmental variables are indicative of environmental control of skeletal Mg content. Additionally, this study aimed to build a solid database of Mg concentrations in the skeletons of Arctic echinoderms, which will act as a baseline for future investigations. 2. Study area The Barents Sea is a shallow continental shelf sea that covers ~1.6 million km2 (Jakobsson et al., 2004). The sea is bounded by the Arctic Ocean to the north and by Norway and Russia to the south. The maximum depth of approximately 500 m is located at the western boundary (Bjørnøyrenna), although the average depth is 230 m, and several basins are between 50 and 200 m. The hydrographic conditions are the result of interactions between the bottom topography and currents. The bottom sediments are variable, with a dominance of finer mud and silt in deeper areas and stony and sandy substrates with mollusc shell fragments on shallower banks (Vinogradova and Litvin, 1960).

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The Barents Sea is a transition zone between the salty and warm Atlantic waters and less saline and colder water masses from the Arctic (Loeng and Drinkwater, 2007). The warmer (T > 2
C, S > 35) Atlantic source water enters the Barents Sea between Bear Island and northern Norway and keeps the southern parts of the sea relatively warmer and ice free throughout the year. The colder Arctic water masses (T < 0
C, 34.3 < S < 34.7) dominate in the northern Barents Sea, and the border between the Arctic and Atlantic waters, called the Polar Front, is stable and shaped by the bottom topography in the western region (Loeng and Drinkwater, 2007). The eastern part of the sea is more variable depending on the strength of the Atlantic water inflow, which is influenced, among other variables, by wind conditions. The Arctic waters enter the northern parts of the Barents Sea along two main routes: between Spitsbergen and Franz Joseph Land and, to a larger extent, through a wide opening between Franz Joseph Land and Novaya Zemlya (Loeng, 1991). In winter, the northern parts of the sea are seasonally icecovered, and the maximum extent of the ice (~60%) occurs in March or April. The minimum ice coverage (0e30%) is observed in AugusteSeptember (Loeng and Drinkwater, 2007). The distribution of chlorophyll a in the Barents Sea changes seasonally, with very low concentrations at all depths in March (0.04 mg m3) and maximum levels during spring blooms in May (6e14 mg m3) (Reigstad et al., 2002). In the present study, all stations spanned a range of environmental conditions from the shallow depths of Svalbard Bank (station 8e74 m) to a maximum depth of 366 m (station 2) to the south

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from Sørkapp. The lowest salinity (34.34) and bottom temperature (1.37
C) were found near the east coast of Edgeøya, while the highest salinity (35.05) was found in the eastern part of the study area, and the highest bottom temperature (3.80
C) was noted in the shallow station located in Svalbard Bank (Fig. 1, Table 1). In summary, differences in seawater temperature (mainly depthrelated) among the sampled stations were found, although salinity appeared to be relatively stable. 3. Materials & methods 3.1. Sample collection and preparation The echinoderm specimens were collected using bottom trawling at 23 stations located in the western and northern parts of the Barents Sea (74
40 Ne79
55 N, 15
02 E  37
51 E, Fig. 1). Bottom water salinity and temperature were measured with CTD at the same time and locations as the bottom trawl stations. Details of the physical and chemical properties of the seawater at ~5 m above the seafloor at each station are presented in Table 1. All samples were obtained during the cruise of R/V Johan Hjort (Institute of Marine Research, Bergen, Norway) in August and September 2015. After collection, echinoderms were separated from other benthic invertebrates, washed, identified to the species level on board the vessel, and then stored at 20
C. In the laboratory (Institute of Oceanology Polish Academy of Sciences, Sopot, Poland), each individual was measured using a slide caliper (asteroids and ophiuroids: R1 ¼ length of longest arm, R2 ¼ radius of disc; other taxa:

Fig. 1. Sampling stations in the Barents Sea, showing water depth (right scale); for details see Table 1.

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A. Iglikowska et al. / Marine Environmental Research xxx (2017) 1e12

Table 1 Geographical location, sampling dates, depths, and physical and chemical properties of bottom seawater at sampling stations. Station

Latitude N

Longitude E

Date of collection

Water depth [m]

Temperature [
C]

Salinity

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23

76
32.97 75
58.87 75
34.03 75
16.67 74
41.80 76
31.08 76
28.34 76
21.38 76
16.13 75
19.13 76
25.04 76
27.52 77
06.27 77
00.10 77
34.01 78
09.63 78
13.33 78
15.64 78
16.29 78
48.05 78
46.95 79
22.49 79
55.16

15
02.97 15
45.10 18
37.80 25
41.68 26
03.12 30
10.49 27
47.94 22
53.21 20
26.18 32
37.83 37
33.48 35
09.04 30
29.33 37
51.65 25
14.18 37
42.90 33
24.69 30
10.36 27
10.45 36
09.77 33
14.67 27
29.92 28
41.05

27-08-2015 27-08-2015 28-08-2015 29-08-2015 29-08-2015 04-09-2015 04-09-2015 05-09-2015 07-09-2015 13-09-2015 14-09-2015 14-09-2015 17-09-2015 17-09-2015 17-09-2015 18-09-2015 19-09-2015 19-09-2015 19-09-2015 21-09-2015 21-09-2015 22-09-2015 23-09-2015

177 366 114 183 297 289 131 74 254 267 244 243 211 181 128 123 179 309 308 226 252 306 306

3.1623 0.3411 3.4798 1.3156 2.7155 1.7790 1.0682 3.8028 0.0258 1.4473 1.6543 1.7684 0.8393 1.2327 1.3695 0.2919 1.3073 0.2967 0.2294 1.0261 0.7055 0.6517 1.1504

34.9765 34.8919 34.9936 34.9380 35.0329 35.0181 34.8693 34.5612 34.8940 35.0386 35.0462 35.0462 34.9012 34.4834 34.3408 34.7368 34.9351 34.9106 34.9023 34.9261 34.4618 34.8205 34.8353

h ¼ height, ø ¼ diameter, see Appendix) and dried for 48 h at 60
C. For further analysis, only specimens of similar size (within species) were taken into account to avoid the potential influence of ontogenetic change on the variability in magnesium concentrations in the skeleton. All skeletal parts were carefully separated under microscope from the soft body parts and organic matter and then cut into pieces using a razor blade. Arms after regeneration were not taken into consideration in further analyses. Because variability in the Mg content among skeletal body parts in echinoids has been confirmed by several authors (e.g. Weber, 1969, 1973; Smith et al., 2016a), in the present study, the spines, Aristotle's lanterns and tests of sea urchins were analysed separately. In all comparisons among species of sea stars, brittle stars and sea lilies, the same part of the skeleton (i.e., arm) was used for magnesium measurements, but not in sea cucumbers, in which, depending on the species, calcareous rings (Myriotrochus rinkii) or the calcified body wall (Psolus phantapus) were sampled. For analysis, each sample was ground into fine powder using an agate mortar and pestle. No bleaching technique was used before mineralogical analyses (see Smith et al., 2016b).

beam. Y2O3 was used as an external standard to calibrate the angular linearity of the detector, and the calibration curve was fitted with a least-squares cubic spline function. The magnesium content in calcite was calculated from the position of the d104 peak assuming a linear change in d104 with composition. A linear relationship between d104 and MgCO3 content exists between 0 and 20 mol% MgCO3 in calcite (e.g. Mackenzie et al., 1983), and all measurements of this study fall within this validated range. The analytical error is 0.2 mol% MgCO3 based on replication measurements. 3.3. Statistical analyses Differences in skeletal MgCO3 concentration among echinoderm classes and species and stations were analysed using the nonparametric Kruskal-Wallis test following an a priori diagnostic test for a normal distribution of the data by means of the ShapiroWilk test. Spearman's correlation test was performed to assess relationships between the MgCO3 content in echinoderm skeletons and size. All statistical computations were run with STATISTICA 10 (StatSoft Inc., 2011).

3.2. Analysis for magnesium 4. Results The mineral composition of the calcified skeleton samples was determined at the Natural History Museum, London. The powdered samples were mixed with acetone, and a drop of the sampleacetone suspension was placed onto a zero-background holder (flat sapphire substrate). The dried samples were analysed with an Enraf Nonius diffractometer (PDS120) equipped with a cobalt source, a germanium 111 primary monochromator and an INEL 120
curved position sensitive detector. The X-ray source was operated at 40 KV and 40 mA. Slits after the monochromator were set to 0.24  5 mm to confine the X-ray beam to pure Co Ka1 radiation. The samples were analysed in reflection mode with a fixed tube-sample-detector geometry and an angle of 6
between the incident beam and sample. The samples were rotated during the measurements to increase the number of crystallites in the X-ray

A total of 235 measurements of magnesium concentration in echinoderm's skeletons were compiled, including measurements from five classes, 30 species and 216 specimens (Appendix). In all studied echinoderms, the skeleton was consistently high-Mg calcite, and the mean skeletal carbonate mineralogy was 11.4 ± 2.0 SD (standard deviation) mol% MgCO3, ranging from 4.6 to 17.9 mol% MgCO3. The lowest content of MgCO3 was recorded for Strongylocentrotus droebachiensis (echinoid, sample ID: SD188, spines) and the highest in Gorgonocephalus arcticus (ophiuroid, GA98, arm, Appendix). The content of MgCO3 in particular echinoderm classes showed the following order: Asteroidea (mean 12.4 mol% MgCO3 ± 1.0 SD) > Ophiuroidea (11.8 ± 1.7) > Crinoidea

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Fig. 2. Mean, standard error and ranges of skeletal MgCO3 contents in studied echinoderm species representing all five classes: A ¼ Asteroidea, O ¼ Ophiuroidea, H ¼ Holothuroidea, E ¼ Echinoidea, C ¼ Crinoidea.

(10.5 ± 0.6) > Holothuroidea (9.7 ± 1.3) > Echinoidea (8.2 ± 2.0); however, the latter three classes were represented by only one (Crinoidea) or two species (Holothuroidea, Echinoidea). Differences in MgCO3 content among classes were statistically significant (Kruskal-Wallis H ¼ 106.2, p < 0.001). Closely related species (i.e., species of the same genus) were characterised by similar concentrations of MgCO3 in skeletal calcite (Fig. 2). In asteroids, we found statistically significant differences in skeletal magnesium content among the studied species (KruskalWallis: H ¼ 17.1, p ¼ 0.009, Fig. 2). The lowest concentrations were noted in Poraniomorpha tumida (mean 11.5 mol% MgCO3 ± 0.5 SD) and the highest levels in Pontaster tenuispinus (13.1 ± 1.2). Statistically significant differences in magnesium content were even more pronounced for ophiuroid species (H ¼ 47.5, p < 0.001, Fig. 2). Among the brittle stars, Ophiocten sericeum was characterised by the lowest MgCO3 concentrations in the skeleton (7.4 mol% MgCO3 ± 0.5 SD), and Gorgonocephalus eucnemis showed the

highest values (14.0 ± 0.4). In asteroids (all studied species), a positive correlation between MgCO3 content and arm length was observed (Spearman's correlation R ¼ 0.39, p < 0.05). Additionally, there was also a positive relationship with disc radius (R ¼ 0.25, p < 0.05). Similarly, in ophiuroids, a positive relationship was found between MgCO3 concentration and both arm length (R ¼ 0.48, p < 0.05) and disc radius (R ¼ 0.56, p < 0.05). In echinoids, particular body parts were analysed regarding their MgCO3 concentrations. Statistically significant differences in MgCO3 content were confirmed among the spines, lantern and test, and this pattern was revealed for both studied echinoid species (S. droebachiensis: H ¼ 9.5, p ¼ 0.009; S. pallidus: H ¼ 9.8, p ¼ 0.007). Lower MgCO3 values were observed in echinoid spines (S. droebachiensis: mean 5.9 mol% MgCO3 ± 1.0 SD; S. pallidus: 5.8 ± 0.9), and higher values were observed in the lantern (S. droebachiensis: 9.0 ± 0.5; S. pallidus: 9.9 ± 0.9) and test

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stations (Fig. 3). Statistically significant differences in skeletal MgCO3 concentrations among particular stations were confirmed for the crinoid Heliometra glacialis (H ¼ 9.95, p ¼ 0.019), with the highest mean MgCO3 concentrations at station 14 (10.9 mol%) and the lowest at station 21 (10.1). Those stations differed in depth (14e181 m, 21e252 m, respectively), but the in situ snapshot measurements of salinity and temperature values were comparable (Table 1). Differences in MgCO3 content were also found in the sea star Pontaster tenuispinus (H ¼ 14.3, p ¼ 0.006), with the lowest values (mean 12.1 mol%) observed at the shallower station 15 (128 m) and the highest contents (14.9) at the deeper station 18 (309 m). No differences in MgCO3 content were found in the sea star Ctenodiscus crispatus (H ¼ 8.1, p ¼ 0.089) or the two brittle star species Ophiopholis aculeata (H ¼ 9.4, p ¼ 0.052) and Ophiura sarsii (H ¼ 5.8, p ¼ 0.215) (Fig. 3). Furthermore, no relationship was found between depth and MgCO3 concentration in the skeletons of the studied species. 5. Discussion 5.1. Mg concentration & taxonomic group We found statistically significant differences in MgCO3 concentrations among particular echinoderm classes and the selected Arctic species. The highest contents were observed in asteroids (number of specimens N ¼ 97), followed by ophiuroids (81), crinoids (20), and holothuroids (7), with the lowest levels in echinoids (10). This pattern, with the highest MgCO3 concentrations in sea stars and the lowest in sea urchins, is consistent with results published by Chave (1954), Weber (1969), McClintock et al. (2011) and Iglikowska et al. (under review). In this study, we also observed that representatives of different species collected from the same station, and thus having developed under the same environmental conditions, showed different, species-specific concentrations of MgCO3 in the skeleton. This result suggests that echinoderm species can exert biological control on Mg incorporation into the skeleton. There might be several drivers that contribute to species- or class-dependent Mg concentrations in the skeleton, including different morphologies of the skeleton, different concentrations of organic material, different exposures to ambient conditions and different life traits of particular species/groups. 5.2. Mg concentration & skeleton morphology

Fig. 3. Box and whiskers plots showing differences in MgCO3 concentrations in skeletons of selected echinoderm species between stations.

(S. droebachiensis: 8.8 ± 0.5; S. pallidus: 9.7 ± 2.2). For five echinoderm species, the MgCO3 concentration in the skeleton was compared for specimens collected from different

The structure and development of echinoderm skeletons differ and are characteristic of particular classes. This attribute of particular classes, as already mentioned, might be a key factor contributing to the observation of class- and often species-specific Mg concentrations. In holothuroids, the skeleton consists of small, isolated ossicles that are dispersed throughout the body wall and a calcareous ring supporting the oesophagus (Kerr and Kim, 2001). The endoskeleton of crinoids is composed of numerous calcareous ossicles arranged to form arms, cirri, pinnules and stalks, which are characteristic for the group (Meyer, 1971). In echinoids, the heavily calcified skeleton includes spines, Aristotle's lantern and the test and is thus much more complex compared to those of representatives of other classes. While the echinoid body is primarily calcareous, the body wall in sea stars contains calcite ossicles and organic connective tissue in roughly equal proportions (O'Neill, 1989). The skeleton of ophiuroids includes an endoskeleton in the form of highly calcified vertebrae

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and functionally external shields, spines and primary plates of the disc (Hendler, 1978). Moreover, in each class, a different set of specific organic macromolecules is associated with the calcified skeleton and controls skeleton formation and magnesium incorporation into the calcite lattice (e.g. Veis et al., 2011; Gorzelak et al., 2013). On the other hand, all echinoderms use the same biomineralisation mechanisms with similar micro/nanostructure of stereom, morphogenesis and unique genetic signature. In the present study, we found statistically significant differences in skeletal Mg content among classes, but species representing the same class showed similar values, which may suggest an association between skeletal morphology and skeletal Mg content. Admittedly, we have not examined the skeletal organic material, but interspecific differences in the distribution, concentration and nature of organic macromolecules are likely key drivers. However, observed differences in Mg concentrations, to some extent, may be also related to differences in growth rates, physiology and others. 5.3. Mg concentration & exposure to seawater In the present study, echinoids showed the lowest Mg contents in the skeleton, whereas asteroids were characterised by the highest Mg levels. The representatives of each echinoderm class possess skeletons that are differently exposed to the impacts of ambient seawater conditions. The components of the echinoid skeleton are only covered by a thin epidermal layer and are thus highly influenced by environmental changes compared to other echinoderm classes. Even the ossicles of Aristotle's lantern are located inside the peripharyngeal coelom, which is in direct contact with seawater (Ebert, 2013). Echinoids are likely to face higher expenditures in terms of producing and maintaining their complex and heavily calcified skeletons, and this is easier with lower skeletal Mg contents. In asteroids, the skeletal tissue is protected by skin and layers of connective tissue and is thus less prone to dissolution due to the impacts of seawater. On the basis of our results, we observed the trend that the heavily calcified skeletons of echinoids and crinoids, which are more exposed to ambient seawater, have lower concentrations of MgCO3, whereas the less calcified endoskeletons of asteroids and ophiuroids, which are more isolated inside the body, tend to incorporate higher magnesium contents. 5.4. Variability in Mg content within single specimen There is also further evidence that echinoderms can biologically regulate their skeletal Mg contents. In present study, we observed that echinoids were characterised not only by the lowest concentrations of MgCO3 but also by the highest variability in magnesium content within a single specimen. In this study, significant differences in magnesium content among the body parts of echinoid species were found, with the lowest concentrations in spines and higher levels in echinoid tests and lantern parts, and the MgCO3 concentrations in tests exceeded those in spines by an average of 3.38 mol%. Other studies (e.g. Raz et al., 2003; Alvares et al., 2007; Veis et al., 2011) reported that the patterns of amino acids in coronal (test) plates and spines are different. These findings suggested a close association between the distribution and concentration of Mg and organic components in the skeleton (e.g. Veis et al., 2011; Gorzelak et al., 2013); therefore, the biological effects seem to be evident. Thus, genetic modulation can shape the synthesis of organic macromolecules and indirectly

7

control the different magnesium concentrations in different body parts. 5.5. Mg concentration & mechanical properties Within each echinoderm class, the skeleton has a different origin, shape, level of complexity, content of organic material and even function. On the other hand, the magnesium content is a parameter closely associated with skeletal mechanical properties; therefore, differences in magnesium concentrations among classes seem to be a natural consequence of other, aforementioned differences. Calcareous skeletal components are designed to be hard and stiff, wherein components rich in the mineral magnesium provide strength and organic material contributes to ductility (Currey, 1999). The resulting skeleton made of composite material is characterised by mechanical properties that surpass those of pure, monolithic calcite (Meyers et al., 2008). In echinoids, the skeleton plays a role in movement, food gathering and protection against predators. The well-developed, Mg-rich test plates completely cover the soft body parts of the animal and form a strong armour. The highest Mg contents in sea urchins are reported for tooth tips (e.g. Veis et al., 2011), increasing mechanical hardness, which is particularly important in scraping food from hard rock €rkel and Gorny, 1973). In echinoid spines, the heterosurfaces (Ma geneous distribution of Mg impedes crack propagation and enhances fracture resistance (Magdans and Gies, 2004; Wilt et al., 2003; O'Neill, 1989). However, Moureaux et al. (2010) claimed that the spines hardness did not correlate with Mg concentration, and structural aspects (e.g. degree of crystallinity or crystal domain volumes) play the major role in hardness properties. The lower concentrations of Mg were observed in holothuroid skeletons, which are strongly reduced and play a minor role in locomotion and feeding. The skeleton of asteroids consists of articulated ossicles embedded in the organic material of the body wall and serves not only in a supporting function but is also involved in movement. Moreover, the combination of Mg-rich calcareous ossicles and collagen connective tissue enable high energy absorption without fracturing (Currey, 1999). Ophiuroid adult skeletons include articulated vertebrae located inside the body that allow the movement of arms and external calcified shields for body protection, but the latter are less Mg-rich due to higher exposure to ambient seawater conditions. In all echinoderm classes, the concentration of Mg in the skeleton increases with distance from the ambient seawater because highly exposed skeletal parts are more prone to dissolution pressure (Smith et al., 2016a). In addition, the logical end result is therefore that echinoderms precipitate in their skeletons the hardest mineral possible. 5.6. Mg concentration & species size In this study, the MgCO3 concentration was positively related to species size (i.e., average size of individuals within species), which was confirmed for both asteroids and ophiuroids. In larger sea stars (Solaster endeca, Pontaster tenuispinus) and brittle stars (Gorgonocephalus arcticus, G. eucnemis), we found concentrations of MgCO3 higher than 14 mol% (Appendix). For larger species, harder and stiffer skeletons made of magnesium-rich calcite may enhance their mechanical properties. However, another possible explanation is that in larger species of sea stars and ophiuroids, the endoskeleton is protected by thicker skin and is thus more isolated from ambient conditions than that of smaller species. Therefore, the high concentration of MgCO3 in larger echinoderm species is

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A. Iglikowska et al. / Marine Environmental Research xxx (2017) 1e12

likely to be a compromise between the benefits of having a strong skeleton and the energetic constraints of maintaining a more soluble, magnesium-rich skeleton in the unfavourable conditions of Arctic seawaters. However, this result is difficult to interpret when there are no data on changes in skeletal MgCO3 concentrations within a given species during its development (ontogeny). Metabolic activity changes depend on the developmental stage, and variability in MgCO3 contents due to ontogenetic change is therefore likely. If juveniles become adults in about the same time during the Arctic summer, then the large species have grown faster, and this variation in growth rate may result in differential incorporation of Mg. 5.7. Mg concentration & environmental factors In the present study, we examined the concentration of Mg in the skeletons of particular species collected at stations that differed in environmental conditions. For three studied echinoderm species, we reported no statistically significant differences in magnesium concentration in the skeleton among stations. For the crinoid H. glacialis and asteroid P. tenuispinus, differences appeared to be significant, but relationships with depth and the detected in situ physicochemical properties of seawater remained obscure. From station 14, we collected six echinoderm species representing all five classes. Echinoderms collected at this station showed quite similar magnesium contents, ranging from mean 11.2 mol% MgCO3 ± 1.2 SD (Ophiopholis aculeata) to 12.6 ± 0.8 (Icasterias panopla), and they were influenced by the same environmental conditions. Deeper station 23 was located in the northern Barents Sea, and in this case, echinoderm species collected from this station differed significantly in MgCO3 skeletal concentration (the lowest contents in Ophiocten sericeum: 7.41 ± 0.5 and the highest values in Ophiura sarsii: 12.67 ± 0.6). This result may suggest that accumulation of Mg in the echinoderm skeleton is primarily determined by biological factors that are specific to particular species or higher taxon and that the effects of ambient seawater conditions seem to have a less significant impact. However, analysing the effects of measured in situ physicochemical seawater parameters on the chemical composition of the skeleton causes some difficulties. The water temperature may vary throughout the year depending on the season and depth, and echinoderms are mobile organisms, meaning that they can change depth and thus the experienced temperature regime, even several times a year. Furthermore, the dependency of Mg concentrations on water temperature may differ among classes or even at the species-specific level. Therefore, it is difficult to obtain reliable results concerning relationships between water temperature and skeletal magnesium concentration in a field study. The skeletal Mg content on the scale investigated in this study seems to not be controlled by the chemical or physical properties of water masses. However, a correlation between water temperature and skeletal Mg content is readily apparent over a larger scale when specimens from different latitudes are analysed. Generally, tropical species contain more MgCO3 in skeletal calcite than temperate forms, which in turn exhibit higher levels than polar species (Mackenzie et al., 1983; Smith et al., 2016a). Indeed, the Arctic species examined in this study have lower Mg concentrations on average compared to species from temperate or tropical latitudes (e.g. Weber, 1969, 1973). However, McClintock et al. (2011) recorded quite high MgCO3 values for Antarctic sea urchins (10.7 mol%),

brittle stars (14.3 mol%) and sea stars (14.6 mol%). On the other hand, not only does water temperature decrease with latitude but also other seawater parameters, such as the calcium carbonate saturation state (e.g. Feely et al., 2004; Andersson et al., 2008). The solubility of CaCO3 varies inversely with water temperature, and consequently polar regions are less saturated than lower latitudes. Calcium carbonate solubility also varies with depth and pressure, being more soluble at greater depths (e.g. Feely et al., 2004; Andersson et al., 2008). In summary, the effects of environmental conditions on the skeletal Mg content are more pronounced when we take species into consideration that were collected from geographically distant locations and/or locations characterised by dramatically different physicochemical conditions. In this study, the seawater environment was less variable and differences in physicochemical conditions were subtler, and therefore the biological control appeared to have a more decisive role in shaping the Mg concentrations in echinoderm skeletons. Based on results of this study, it is evident that the content of magnesium in a calcified skeleton is characteristic for a particular echinoderm class and is thus genetically controlled to a large extent (e.g. Solovjev, 2014). According to Solovjev (2014), the strict genetic control of Mg concentration in echinoids likely occurs at lower taxonomic levels and is even characteristic among genera. As we have suggested, the observed species-specific variation in skeletal Mg content seems to be genetically controlled, yet the drivers behind it are very complex, and its level of influence is far from fully understood. Therefore, there is a need for further studies to reveal the possible relationships between skeletal magnesium concentrations and, for example, feeding type, life traits or habitat. In the Barents Sea echinoderm fauna is numerous and highly diverse nevertheless the low water temperatures are likely to hamper incorporation and maintaining high Mg contents in their skeletal elements. Echinoderms are food of many other invertebrates and fishes, thus they are an important part of trophic chain, and play a role in global elements turnover. Progressing hypercapnia of Arctic seas may lead to changes in species composition and dominance structure of calcifying invertebrates. Echinoderms with weaker skeleton will be more vulnerable to predation pressure and interspecific competition. In extreme cases some species, or even groups of species, may be displaced by other organisms. Exclusion of certain species consequently will deprive of food or will limit access to food for species representing higher trophic levels (such as fish having economic significance for people). This can have a decisive influence on food web destabilisation and the future of the Arctic ecosystem. 6. Concluding remarks In the Barents Sea, Mg concentrations in echinoderm skeletons are characteristic for particular echinoderm classes, which, we assume, is a result of biological control. The generally lower values of Mg concentrations observed in the skeletons of Arctic echinoderms in comparison to echinoderms from lower latitudes are most likely related to large-scale environmental characteristics of the investigated habitat, with the low water temperature likely a dominant factor. Our results suggest that the concentration of MgCO3 in skeletal calcite in the studied material is shaped by natural selection, which tends to find a balance among the mechanical properties of the skeleton, the solubility of skeletal minerals and precipitation costs in the environmental conditions

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characteristic of a particular geographic region. It seems that the subtler effects of abiotic factors such as salinity or the Mg/Ca ratio of ambient seawater are highly complex (Weiner and Dove, 2003: “Each proxy may have its own vital effect story”) and that their influence is usually more pronounced when those water mass characteristics are more drastically differentiated than in the study area covered by this investigation. Therefore, as previously emphasized by some authors (Gorzelak et al., 2013, 2016), applying the skeletal Mg/Ca ratio in palaeoenvironmental studies, especially using the same algorithm correcting the effect of vital effect for all echinoderm classes, should be carefully planned and often cautiously undertaken. The reliable data regarding relationships between abiotic environmental factors and skeletal Mg contents in echinoderms, which seems to be very complex, can be obtained only under the controlled conditions of laboratory experiments.

Acknowledgements The research leading to these results received funding from the Polish-Norwegian Research Programme operated by the National Centre for Research and Development under the Norwegian Financial Mechanism 2009e2014 in the frame of Project Contract No Pol-Nor/196260/81/2013. We would like to express our deep thanks to Lis L. Jørgensen (Institute of Marine Research, Tromsø, Norway) for facilitating access to ship-based trawling operations in Barents Sea.

9

(continued ) ID

Species

CC28 CC29 CC30 CC31 CC32 CC33 CC34 CC35

Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus

Station

MgCO3 mol%

R1

R2

23 23 23 13 13 13 13 13

10.636 12.754 13.496 12.065 11.521 11.547 11.071 12.137

17.20 18.58 17.14 21.42 18.96 21.50 21.11 19.94

9.90 9.03 8.66 8.23 9.42 11.73 10.69 10.70

HP36

Hippasteria phrygiana

3

12.768

80.00

47.00

HY37 HY38 HY39

Hymenaster pellucidus Hymenaster pellucidus Hymenaster pellucidus

21 21 21

11.120 10.813 11.765

17.30 12.21 11.45

10.84 7.02 6.11

IP40 IP41 IP42 IP43 IP44

Icasterias Icasterias Icasterias Icasterias Icasterias

14 14 14 14 14

12.282 13.051 13.362 12.905 11.223

102.63 97.74 98.77 99.17 98.83

8.94 10.27 11.67 8.41 10.72

KH45 KH46 KH47

Korethraster hispidus Korethraster hispidus Korethraster hispidus

21 21 21

11.785 10.934 11.441

12.02 18.79 12.00

7.10 7.42 8.11

LF48 LF49

Lophaster furcifer Lophaster furcifer

19 19

11.083 11.209

14.51 9.22

4.96 3.10

crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus

panopla panopla panopla panopla panopla

Appendix. MgCO3 concentrations in asteroids' skeletons and size details in mm (R1 ¼ length of longest arm, R2 ¼ radius of central disc)

Appendix. MgCO3 concentrations in asteroids' skeletons and size details in mm (R1 ¼ length of longest arm, R2 ¼ radius of central disc).

ID

Species

AR1 AR2 AR3 AR4 AR5

Asterias Asterias Asterias Asterias Asterias

CP6 CP7 CP8 CP9 CP10

Crossaster Crossaster Crossaster Crossaster Crossaster

CC11 CC12 CC13 CC14 CC15 CC16 CC17 CC18 CC19 CC20 CC21 CC22 CC23 CC24 CC25 CC26 CC27

Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus Ctenodiscus

rubens rubens rubens rubens rubens papposus papposus papposus papposus papposus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus crispatus

Station

MgCO3 mol%

R1

R2

7 7 7 7 7

13.462 12.611 11.690 11.753 11.636

13.97 14.39 14.15 13.29 12.80

3.81 3.21 4.50 3.63 3.07

6 6 6 6 6

12.611 12.854 12.374 12.888 11.533

27.74 16.77 14.99 14.92 13.09

11.93 6.48 7.01 6.78 6.48

18 18 18 18 18 12 12 12 12 12 9 9 9 9 9 23 23

13.017 12.668 13.351 11.163 13.299 12.311 12.122 12.383 11.650 11.593 11.776 11.899 11.109 11.599 11.570 12.414 12.260

21.84 21.24 20.24 20.23 21.41 18.78 17.41 17.11 17.98 19.17 19.02 18.34 17.98 18.63 19.78 17.69 18.51

12.41 9.17 12.55 10.12 12.02 9.80 9.43 10.29 10.11 9.10 11.08 10.19 10.24 11.68 10.29 9.10 9.24

ID

Species

PT50 PT51 PT52 PT53 PT54 PT55 PT56 PT57 PT58 PT59 PT60 PT61 PT62 PT63 PT64 PT65 PT66 PT67 PT68 PT69 PT70 PT71 PT72 PT73 PT74

Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster Pontaster

PO75 PO76 PO77 PO78 PO79

Poraniomorpha Poraniomorpha Poraniomorpha Poraniomorpha Poraniomorpha

PM80

Pteraster militaris

tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tenuispinus tumida tumida tumida tumida tumida

Station

MgCO3 mol%

R1

R2

15 15 15 15 15 14 14 14 14 14 9 9 9 9 9 18 18 18 18 18 22 22 22 22 22

13.887 11.040 11.819 11.017 12.668 12.751 12.577 12.097 12.671 11.679 14.166 13.102 13.242 11.736 13.231 13.593 15.679 15.031 14.966 15.307 12.768 12.791 12.231 13.468 12.923

77.15 49.40 52.16 46.00 34.27 41.50 29.27 57.77 44.50 30.53 45.20 72.72 48.06 64.34 63.52 48.00 39.83 62.56 36.65 40.40 37.52 47.23 54.64 37.19 43.96

13.77 13.91 13.34 13.34 12.40 11.84 12.13 12.39 12.61 11.59 11.14 12.05 12.23 12.47 11.97 11.01 13.31 13.09 11.01 11.62 13.34 14.13 12.07 11.13 11.74

16 16 16 16 16

11.338 10.934 11.733 12.214 11.347

28.83 24.04 24.42 21.68 19.08

17.52 15.39 12.90 13.12 8.67

3

12.785

20.02

9.66

(continued on next page)

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(continued )

(continued )

ID

Species

Station

MgCO3 mol%

R1

R2

ID

Species

PM81 PM82 PM83 PM84

Pteraster Pteraster Pteraster Pteraster

militaris militaris militaris militaris

3 3 3 3

13.767 12.237 12.391 12.285

23.65 19.13 19.17 19.79

11.91 11.29 9.77 8.89

PB85 PB86 PB87 PB88

Pteraster Pteraster Pteraster Pteraster

obscurus obscurus obscurus obscurus

7 7 7 7

12.871 12.982 12.445 13.000

31.44 26.25 16.14 11.52

21.71 18.36 10.26 9.73

PP89 PP90 PP91 PP92

Pteraster Pteraster Pteraster Pteraster

pulvillus pulvillus pulvillus pulvillus

9 9 9 9

13.901 11.733 12.460 11.066

39.78 27.20 20.75 21.02

19.57 17.31 14.51 12.39

OA132 OA133 OA134 OA135 OA136 OA137 OA138 OA139 OA140 OA141 OA142 OA143 OA144

Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis

SE93 SE94

Solaster endeca Solaster endeca

18 18

14.149 12.771

101.73 105.83

36.26 38.36

SG95 SG96

Solaster glacialis Solaster glacialis

14 14

13.576 10.954

90.00 85.00

34.07 32.09

SS97

Solaster syrtensis

21

12.468

115.00

50.00

aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata

Station

MgCO3 mol%

R1

R2

16 16 16 4 4 4 4 4 23 23 23 23 23

11.813 11.160 11.928 10.412 10.110 11.415 11.031 11.043 12.097 12.228 11.404 12.480 12.391

41.51 36.63 33.14 34.29 20.13 18.93 20.00 27.96 31.55 20.60 47.39 38.42 25.86

8.28 8.06 7.57 8.80 8.68 9.81 9.86 8.63 8.15 7.92 7.97 7.23 7.51

Appendix. MgCO3 concentrations in ophiuroids' and holothuroids' skeletons and size details in mm (R1 ¼ length of longest arm, R2 ¼ radius of central disc, for M. rinkii ¼ diameter of ring, for P. phantapus ¼ body length and height)

Appendix. MgCO3 concentrations in ophiuroids' skeletons and size details in mm (R1 ¼ length of longest arm, R2 ¼ radius of central disc)

ID

Species

Station

MgCO3 mol%

R1

R2

GA98 GA99 GA100 GA101 GA102

Gorgonocephalus Gorgonocephalus Gorgonocephalus Gorgonocephalus Gorgonocephalus

arcticus arcticus arcticus arcticus arcticus

8 8 8 8 8

17.897 14.485 14.943 14.573 15.454

80.00 70.00 130.00 90.00 90.00

30.53 27.67 32.54 28.20 32.47

GE103 GE104 GE105 GE106

Gorgonocephalus Gorgonocephalus Gorgonocephalus Gorgonocephalus

eucnemis eucnemis eucnemis eucnemis

18 18 18 18

13.667 13.744 13.935 14.602

78.71 118.74 70.87 73.70

33.90 31.16 43.92 49.53

GL107 GL108 GL109

Gorgonocephalus lamarckii Gorgonocephalus lamarckii Gorgonocephalus lamarckii

11 11 11

11.432 13.408 12.008

86.03 85.98 92.87

34.60 44.44 39.58

OB110 OB111 OB112 OB113 OB114

Ophiacantha Ophiacantha Ophiacantha Ophiacantha Ophiacantha

22 22 22 22 22

11.163 11.329 11.553 11.292 11.710

43.32 25.37 48.38 39.99 35.19

6.07 6.74 5.47 5.71 6.11

OP115 OP116 OP117 OP118 OP119

Ophiocten Ophiocten Ophiocten Ophiocten Ophiocten

23 23 23 23 23

7.542 8.133 6.889 7.545 6.932

18.04 9.17 9.66 8.88 15.79

5.47 5.91 5.79 6.41 4.47

OA120 OA121 OA122 OA123 OA124 OA125 OA126 OA127 OA128 OA129 OA130 OA131

Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis Ophiopholis

14 14 14 14 14 15 15 15 15 15 16 16

10.842 11.862 11.656 12.448 9.461 11.885 10.790 10.942 10.707 10.624 10.590 11.146

60.14 39.56 29.68 51.34 47.95 44.62 41.18 49.27 33.37 34.53 42.79 43.56

8.27 8.20 8.32 7.72 8.83 7.91 8.11 8.60 8.51 8.30 8.65 8.18

bidentata bidentata bidentata bidentata bidentata

sericeum sericeum sericeum sericeum sericeum aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata aculeata

ID

Species

Station

MgCO3 mol%

R1

R2

BO145 BO146 BO147 BO148 BO149

Ophiopleura Ophiopleura Ophiopleura Ophiopleura Ophiopleura

borealis borealis borealis borealis borealis

19 19 19 19 19

12.934 12.388 13.308 13.622 12.754

76.45 67.00 29.91 39.73 61.72

17.20 17.64 18.94 17.81 18.08

OG150 OG151 OG152 OG153 OG154

Ophioscolex Ophioscolex Ophioscolex Ophioscolex Ophioscolex

glacialis glacialis glacialis glacialis glacialis

19 19 19 19 19

11.913 11.493 12.039 11.996 11.810

60.70 63.56 67.16 117.27 96.42

6.12 5.87 6.44 5.75 6.31

OS155 OS156 OS157 OS157 OS158 OS159 OS160 OS161 OS162 OS163 OS164 OS165 OS166 OS167 OS168 OS169 OS170 OS171 OS172 OS173 OS174 OS175 OS176 OS177 OS178

Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura Ophiura

1 1 1 1 1 2 2 2 2 2 5 5 5 5 5 10 10 10 10 10 23 23 23 23 23

11.805 11.965 12.145 11.507 12.685 11.570 11.762 12.531 10.762 12.603 11.788 12.074 13.510 10.690 11.324 12.014 10.928 12.328 10.799 11.567 13.040 12.637 12.391 11.799 13.499

21.66 27.36 35.68 33.97 28.96 22.71 16.76 24.35 26.50 20.21 18.55 15.66 19.65 11.54 21.67 10.75 32.94 14.18 25.09 16.01 77.21 74.26 52.49 77.73 52.29

9.33 9.54 9.05 9.55 9.82 10.98 10.01 10.26 11.68 10.32 9.66 8.37 9.23 9.85 9.49 8.61 8.26 8.50 8.55 8.31 9.99 10.41 11.01 10.83 10.59

MR179 MR180 MR181 MR182 MR183 PH184 PH185

Myriotrochus rinkii Myriotrochus rinkii Myriotrochus rinkii Myriotrochus rinkii Myriotrochus rinkii Psolus phantapus Psolus phantapus

17 17 17 17 17 14 14

9.213 8.393 9.651 9.984 8.182 11.467 11.284

6.93 6.77 6.96 6.82 6.69 24.01 20.39

e e e e e 11.42 10.69

sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii sarsii

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11

Appendix. MgCO3 contents in echinoids' and crinoids' skeletons and size details in mm (S ¼ spine, L ¼ Aristotle's lantern, T ¼ test, ø ¼ diameter, h ¼ body height, R1 ¼ arm length)

ID

Species

SD186 SD187 SD188 SD189 SD190 SD191 SD192 SD193 SD194 SD195 SD196 SD197 SD198 SD199 SD200

Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus

droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis droebachiensis

SP201 SP202 SP203 SP204 SP205 SP206 SP207 SP208 SP209 SP210 SP211 SP212 SP213 SP214 SP215

Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus Strongylocentrotus

pallidus pallidus pallidus pallidus pallidus pallidus pallidus pallidus pallidus pallidus pallidus pallidus pallidus pallidus pallidus

HG216 HG217 HG218 HG219 HG220 HG221 HG222 HG223 HG224 HG225 HG226 HG227 HG228 HG229 HG230 HG231 HG232 HG233 HG234 HG235

Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra Heliometra

glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis glacialis

(S) (S) (S) (S) (S) (L) (L) (L) (L) (L) (T) (T) (T) (T) (T)

(S) (S) (S) (S) (S) (L) (L) (L) (L) (L) (T) (T) (T) (T) (T)

Station

MgCO3 mol%

ø

h/R1

3 3 3 3 3 3 3 3 3 3 3 3 3 3 3

6.493 6.276 4.614 5.044 6.970 8.972 8.854 9.395 8.176 9.550 8.044 8.522 8.983 9.277 9.127

35.89 41.55 36.62 34.67 34.33 35.89 41.55 36.62 34.67 34.33 35.89 41.55 36.62 34.67 34.33

20.58 20.76 20.09 21.01 18.80 20.58 20.76 20.09 21.01 18.80 20.58 20.76 20.09 21.01 18.80

2 2 2 2 2 2 2 2 2 2 2 2 2 2 2

5.418 7.059 5.209 6.458 5.038 9.550 10.125 9.464 11.415 9.113 8.338 10.047 13.334 8.571 8.153

47.66 37.45 34.46 31.10 31.05 47.66 37.45 34.46 31.10 31.05 47.66 37.45 34.46 31.10 31.05

25.98 23.28 21.39 19.38 17.32 25.98 23.28 21.39 19.38 17.32 25.98 23.28 21.39 19.38 17.32

14 14 14 14 14 16 16 16 16 16 20 20 20 20 20 21 21 21 21 21

11.077 11.114 10.868 10.572 11.046 10.931 10.615 10.659 10.572 11.687 10.544 10.590 9.832 10.638 9.642 10.311 9.708 10.836 9.274 10.248

19.84 20.88 21.48 19.86 17.43 20.90 21.54 21.59 20.87 19.97 18.91 17.48 19.44 17.62 17.44 20.29 21.05 18.23 18.91 17.32

54.32 62.78 51.64 74.16 40.89 116.01 87.71 103.24 62.78 51.78 45.36 36.22 57.36 49.51 42.69 71.07 66.44 68.43 43.74 43.17

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Please cite this article in press as: Iglikowska, A., et al., Variability in magnesium content in Arctic echinoderm skeletons, Marine Environmental Research (2017), http://dx.doi.org/10.1016/j.marenvres.2017.06.002